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Eastern oysters (Crassostrea virginica) as an indicator forrestoration of Everglades Ecosystems
Aswani K. Volety a,*, Michael Savarese a, S. Gregory Tolley a, William S. Arnold b,Patricia Sime c, Patricia Goodman c, Robert H. Chamberlain c, Peter H. Doering c
aCoastal Watershed Institute, Florida Gulf Coast University, 10501 FGCU Boulevard South, Fort Myers, FL 33965, United Statesb Fish and Wildlife Research Institute, 100 Eighth Avenue SE, St. Petersburg, FL 33701, United StatescSouth Florida Water Management District, 3301 Gun Club Road, West Palm Beach, FL 33406, United States
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6
a r t i c l e i n f o
Article history:
Received 17 March 2008
Received in revised form
28 May 2008
Accepted 17 June 2008
Keywords:
Ecological indicators
Everglades Restoration
Oysters
Water quality
Ecosystem health
a b s t r a c t
The Comprehensive Everglades Restoration Plan (CERP) attempts to restore hydrology in the
Northern and Southern Estuaries of Florida. Reefs of the Eastern oyster Crassostrea virginica
are a dominant feature of the estuaries along the Southwest Florida coast. Oysters are
benthic, sessile, filter-feeding organisms that provide ecosystem services by filtering the
water column and providing food, shelter and habitat for associated organisms. As such, the
species is an excellent sentinel organism for examining the impacts of restoration on
estuarine ecosystems. The implementation of CERP attempts to improve: the hydrology
and spatial and structural characteristics of oyster reefs, the recruitment and survivorship
of C. virginica, and the reef-associated communities of organisms.
This project links biological responses and environmental conditions relative to hydro-
logical changes as a means of assessing positive or negative trends in oyster responses and
population trends. Using oyster responses, we have developed a communication tool (i.e.,
Stoplight Report Card) based on CERP performance measures that can distinguish between
responses to restoration and natural patterns. The Stoplight Report Card system is a
communication tool that uses Monitoring and Assessment Program (MAP) performance
measures to grade an estuary’s response to changes brought about by anthropogenic input
or restoration activities. The Stoplight Report Card consists of both a suitability index score
for each organism metric as well as a trend score (� decreasing trend, +/� no change in
trend, and + increasing trend). Based on these two measures, a component score (e.g., living
density) is calculated by averaging the suitability index score and the trend score. The final
index score is obtained by taking the geometric score of each component, which is then
translated into a stoplight color for success (green), caution (yellow), or failure (red).
Based on the data available for oyster populations and the responses of oysters in the
Caloosahatchee Estuary, the system is currently at stage ‘‘caution.’’ This communication
tool instantly conveys the status of the indicator and the suitability, while trend curves
provide information on progress towards reaching a target. Furthermore, the tool has the
advantage of being able to be applied regionally, by species, and collectively, in concert with
other species, system-wide.
# 2008 Elsevier Ltd. All rights reserved.
avai lable at www.sc iencedi rec t .com
journal homepage: www.e lsev ier .com/ locate /ecol ind
* Corresponding author. Tel.: +1 239 590 7216; fax: +1 239 590 7200.
1470-160X/$ – see front matter # 2008 Elsevier Ltd. All rights reserved.doi:10.1016/j.ecolind.2008.06.005
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6 S121
1. Introduction and background
The Eastern oyster (Crassostrea virginica) once supported a
Native American subsistence fishery prior to and during early
European colonization of North America (Quitmyer and
Massaro, 1999) and today continues to be an important
economic and ecological resource to coastal inhabitants (Ingle
and Smith, 1949; Coen et al., 1999; Gutirrez et al., 2003).Although
not commercially harvested in southern Florida estuaries,
oysters provide habitat for other estuarine species that have
significant recreational and commercial value. Oysters are also
ecologically important: they improve water quality by filtering
particles from the water and serve as prey and habitat for many
other animals (Coen et al., 1999). For example, oyster reefs are
home to gastropod mollusks, polychaete worms, decapod
crustaceans, boring sponges, fishes, and birds. Over 300
macrofaunal species may associate with oyster reefs and over
40 species may inhabit a single oyster bed (Wells, 1961).
In the Caloosahatchee, Loxahatchee, Lake Worth Lagoon,
and St. Lucie Estuaries (Northern Estuaries of the Everglades),
oysters have been identified as a Valued Ecosystem Compo-
nent (VEC; Chamberlain and Doering, 1998a, 1998b). Oysters
are natural components of estuaries along the eastern
seaboard of the U.S. as well as the Gulf of Mexico and were
once abundant in the Northern Estuaries (Systems Status
Report 2007). The Eastern oyster possesses a broad geogra-
phical distribution and wide temperature and salinity toler-
ances (Gunter and Geyer, 1955; Cake, 1983) and is the
dominant species in these oyster-reef communities. Adult
oysters normally occur at salinities between 10 and 30 ppt, but
they tolerate salinities of�2 to 40 ppt (Gunter and Geyer, 1955).
Occasional, short pulses of freshwater inflow can greatly
benefit oyster populations by reducing predator (e.g., oyster
drill, whelk) and parasite (e.g., Perkinsus marinus) impacts
(Owen, 1953), but excessive freshwater inflow may kill entire
populations of oysters (Gunter, 1953; Schlesselman, 1955;
MacKenzie, 1977; Volety et al., 2003; Volety and Tolley, 2005;
Bergquist et al., 2006). Reefs located near the head of an
estuary, where salinities range from 0 to 15 ppt, are sparsely
populated due to frequent flooding and high mortality rates
(Butler, 1954; Volety and Savarese, 2001; Savarese et al., 2003).
Spat recruitment and juvenile growth rates are also low in this
location. Where salinities are between 15 and 20 ppt, popula-
tions are dense, reproductive activity is high, predator
numbers are low, and spat recruitment and growth rates
are high (Shumway, 1996; White and Wilson, 1996). Toward
the higher salinity waters near the mouth of the estuary,
oyster reefs are sparse, spat recruitment and growth are low,
diseases and predators are high, and suitable substrate is often
lacking. Salinity also affects gametogenesis, condition index,
spawning, and disease in oysters (Shumway, 1996). Salinities
<5 ppt impair gametogenesis while normal gametogenesis
occurs above 7.5 ppt; oysters from Texas, for example, showed
suppressed gonadal activity at salinities <6 ppt (Shumway,
1996). Similar trends were observed in Caloosahatchee River
oysters in 2003 in response to regulatory freshwater releases
(Volety, unpublished results).
Additionally, the protozoan parasite P. marinus has deva-
stated oyster populations in the Atlantic (Burreson and Ragone-
Calvo, 1996) as well as in the Gulf of Mexico (Soniat, 1996), where
it is currently the primary pathogen (Dermo disease) of oysters.
Andrews (1988) estimates that P. marinus can kill �80% of the
oysters on a reef. Temperature and salinity influence the
distribution and prevalence of P. marinus with higher values
favoring the parasite (Burreson and Ragone-Calvo, 1996; Soniat,
1996; Chu and Volety, 1997; La Peyre et al., 2003). Laboratory
studies by Chu and Volety (1997) suggest that although
temperature is important, salinity is the most important factor
influencing the disease susceptibility and disease progression
of P. marinus in oysters. High salinities also attract various
predators such as crabs, starfish, boring sponges, and oyster
drills, along with Dermo disease (Butler, 1954; Hopkins, 1962;
Galtsoff, 1964; Menzel et al., 1966; Shumway, 1996; Livingston
et al., 2000). Therefore, the quality (e.g., nutrients, contami-
nants, suspended sediments), quantity, timing, and duration of
freshwater inflow have a tremendous effect on oyster health,
survival, growth, and reproduction, and thus the biological
responses of oysters are directly related to freshwater-influ-
enced environmental conditions.
1.1. Indicator history
Oysters are common throughout the estuarine portions of the
Northern (Caloosahatchee, St. Lucie, Loxahatchee, and Lake
Worth Lagoon) and Southern (Whitewater Estuary, Shark River,
Coot Bay, Oyster Bay, and areas of the Ten Thousand Islands)
Estuaries (Fig. 1). Water management and dredging practices
have had a major impact on the presence, density, and
distribution of oysters within the mesohaline areas of the
Northern and Southern Estuaries. Historically, drainage pat-
terns were characterized by gentle, meandering surface water
flows through rivers, creeks, and sloughs and overland sheet
flow through contiguous marshy areas. This natural system
absorbed floodwater, promoted ground water recharge, assimi-
lated nutrients, and removed suspended materials (ACOE and
SFWMD 2002). As South Florida developed, the canal network,
built as part of the Central and Southern Florida Flood Control
Project, worked very efficiently in preventing floods and
drasticallyalteredthe quantity, quality, timing, and distribution
of freshwater entering the estuaries. Freshwater flow into the
estuaries and their tributaries increased both in volume and
frequency (often to prevent flooding) relative to the pre-
drainage era. This caused rapid, often within a few hours,
changes in salinity resulting in degradation of the biological
integrity of the estuaries. Furthermore, inflow is often too great
in the wet season and too little in the dry season to support a
healthy estuary. Additionally, flood releases and inland runoff
contain numerous contaminants from urban and agricultural
development including excess suspended solids, nutrients,
pesticides, and other Emerging Pollutants of Concern such as
hormones and pharmaceuticals. This results in poor quality
water entering the estuaries.
Although the Caloosahatchee Estuary (Fig. 2) is used as a
specific example below, similar water quality concerns are
present in all Northern and Southern estuaries given the
similarities in watershed alteration. The Caloosahatchee River
is the major source of freshwater for the Caloosahatchee
Estuary (CE) and southern Charlotte Harbor. The river, which
has been transformed into a canal (C-43), conveys both runoff
from the Caloosahatchee watershed and regulatory releases
Fig. 1 – Location of Northern (Caloosahatchee, St. Lucie, Loxahatchee, and Lake Worth Lagoon) and Southern (Whitewater
Estuary, Shark River, Coot Bay, Oyster Bay, and areas of the Ten Thousand Islands) Estuaries in Florida.
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6S122
from Lake Okeechobee. The C-43 canal has undergone a
number of alterations to facilitate this increased freshwater
discharge and improve flood protection: channel straighten-
ing and enlargement, bank stabilization, the development of
an intricate network of ancillary canals within the watershed,
and the addition of three locks and dams. The final down-
stream structure, the W.P. Franklin Lock and Dam (S-79),
demarcates the beginning of the estuary and acts as a barrier
to salinity and tidal action, which historically extended much
farther upstream. All of these alterations to the Caloosa-
Fig. 2 – Sampling locations within the Caloosahatchee Estuary. Locations (PPT = Pepper Tree Point, IC = Iona Cove/Shell
Point, CD = Cattle Dock, BI = Bird Island, KK = Kitchel Key, and TB = Tarpon Bay) are from upstream to downstream along a
salinity gradient.
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6 S123
hatchee River and its watershed have resulted in a drastic
change in freshwater inflow to the ecosystem downstream
resulting in large fluctuations of salinity and water quality that
adversely impact estuarine biota (Chamberlain and Doering,
1998a; Sklar and Browder, 1998).
The dominant biological features in the downstream
portion of the Caloosahatchee River estuary are its numer-
ous mangrove islands and many kilometers of mangrove
shoreline, which are often closely associated with oysters.
Because of its biotic richness and aesthetic appeal, the
Caloosahatchee Estuary supports a wide variety of recrea-
tional and fishery activities with significant economic value.
The natural resources of this area are also impacted by large
freshwater releases and are threatened by long-term shifts
in water quantity and quality (Chamberlain and Doering,
1998b; Doering et al., 2002; Volety et al., 2003). Under current
water management practices, the estuarine portion of the
river is essentially fresh during the wet season due to
freshwater releases and runoff from summer rains (Volety
et al., 2003).
During the dry winter season freshwater releases are
halted and the estuary becomes hypersaline because of its
high ratio of surface area to volume and resultant evaporative
loss. Freshwater releases during summer months flush oyster
larvae downstream to locations that have unsuitable sub-
strate, or create salinity conditions that are unfavorable
(<5 ppt) for larval survival in the estuarine portions of the
river. Oysters in Southwest Florida spawn continuously, with
peak recruitment (spat settlement) occurring May to Novem-
ber. Recruitment near Shell Point and possibly upstream
begins to peak in March, a full 3 months earlier than in San
Carlos Bay, located farther downstream, rendering these
newly settled juveniles vulnerable to large releases from S-
79, which are often made during this period to regulate Lake
Okeechobee water level for flood protection. Large freshwater
flows at this time and during the summer also expose oyster
larvae to lethally low salinities or flush the larvae downstream
to locations where there may not be suitable substrate for
settlement (Volety et al., 2003).
Recent investigations in the CE have estimated the
optimum quantity of freshwater needed to protect key biota.
These VEC species (oysters and sea grasses), help sustain the
ecological structure and function of the estuary by providing
food, living space, and foraging sites for other estuarine
species. Oysters and submerged aquatic vegetation (SAV)
represent VECs in the CE. Proper management (e.g., frequency,
timing, quantity, and quality) of water releases to the estuary
will protect these species and should lead to the restoration of
healthy and diverse estuarine ecosystems.
Work by Tolley and Volety (2005) and Volety et al. (2003)
documents the importance of C. virginica as a VEC. They found
that a greater abundance of decapods and fishes was
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6S124
associated with clusters of live oysters compared to clusters of
dead oysters, and that the structure provided by both living
and dead oyster shells supported a greater abundance than no
shells. Species richness and biomass were also higher for
samples with oyster clusters (dead or live) compared to
controls with no oyster shell (Tolley and Volety, 2005). This
study suggests that the real significance of living oysters to
habitat value lies not only in creating a three-dimensional
structure, but also in maintaining this structure of clusters
through time. In the absence of oyster-reef growth, individual
oysters within a cluster or bed may die, leaving empty
compartments for reef residents, but mass mortality of a
cluster results in the disarticulation and eventual loss of the
oyster shells (Volety et al., 2003; Tolley and Volety, 2005).
Therefore freshwater or habitat alteration unfavorable to
oysters will not only result in decreases in the extent of oyster
reefs and filtration-improved water quality, but also the
species residing on the oyster reefs.
Volety et al. (2003) evaluated adult and juvenile oyster
survival, the prevalence and intensity of disease, and oyster
recruitment success. These responses were compared to
environmental factors including salinity and freshwater flow
from S-79. Oysters grew best at a salinity of 14–28 ppt.
Infection by the oyster pathogen P. marinus increased during
periods of higher salinity and temperature. Field studies
determined that the prevalence of infection was high, but
disease intensity was low, likely resulting from an antag-
onistic interaction between temperature and salinity (i.e., high
summer temperature occurs during the wet season when
salinity is low). Therefore, freshwater releases to diminish P.
marinus are generally not necessary during warm summer
months and could potentially threaten oyster populations
through further reductions in salinity.
In the CE, the greatest oyster growth and recruitment
occurs during the wet season, but slower growth and poor spat
production occur at salinities below 14 ppt. Volety et al. (2003)
found that salinity conditions were best suited for oyster
growth just upstream of Shell Point in the CE; however, this
area is also the most vulnerable to high mortality when large
freshwater releases cause salinity to fall below threshold
tolerance (<5 ppt), sometimes for prolonged periods (>1–2
weeks). These authors further report that although adult
oysters are tolerant of variable salinity, salinities�5 ppt result
in>95% mortality of juvenile oysters. High mortality can occur
when juveniles are exposed to this salinity for just a week
(Volety et al., 2003).
Experimental results indicate that adults are able to tole-
rate salinities as low as 5 ppt for up to 8 weeks, but cannot
tolerate salinities lower than 3 ppt, which can occur at up-
stream portions of the CE when S-79 discharges exceed
4000 cubic feet per second (cfs) (Volety et al., 2003). Therefore,
high discharges can limit survival and abundance in this
region where oysters were historically present. Volety et al.
(2003) indicated that since high spat recruitment, fast growth,
and low disease incidence and intensity are found at
intermediate salinities (10–20 ppt), it is feasible to reestablish
oyster reefs within the CE by strategically deploying oyster
cultch in suitable areas, as long as freshwater releases are
managed to maintain salinity within the range of normal
oyster tolerances (5–35 ppt).
1.2. Comprehensive Everglades Restoration Plan
The implementation of the Comprehensive Everglades
Restoration Plan’s (CERP) Monitoring Assessment Plan
(MAP) will help determine how well CERP is meeting its
restoration goals and objectives. The premise of CERP is that
restoring hydrology in the Northern and Southern Estuaries
will improve the spatial and structural characteristics of
oyster reefs and improve recruitment and survivorship of C.
virginica and associated fauna. The hypotheses below are the
result of a conceptual model of stressors that impact oysters,
oyster reefs, and secondary habitat (Fig. 3; SSR, 2007). The
conceptual model is a product of the known cause and effect
relationships between stressors andC. virginica ecological and
physiological responses from published studies for this
region (cited previously) and elsewhere throughout the
species’ range. Consequently, the hypotheses have withstood
rigorous testing and therefore serve as guideposts for
restoration. Correlations between biological responses and
environmental conditions relative to hydrological changes
contribute to the assessment of positive or negative trends in
restoration. Restoration success or failure related to the
oyster indicator can be evaluated by comparing recent
monitoring efforts and future trends and health status of
oyster reefs in the Northern Estuaries, unaltered or control
estuaries, and model predictions (e.g., Habitat Suitability
Index), as stated in the CERP hypotheses related to the oysters
(CERP Monitoring and Assessment Plan sections 3.3.3.6;
RECOVER 2004, SSR, 2007).
1.3. CERP MAP hypotheses related to the Eastern oysterindicator
The following hypotheses developed for the Eastern oyster
and adopted for CERP-MAP serve as defining criteria for the
evaluation of Everglades Restoration.
� Sudden and drastic changes in the estuarine salinity
envelope can result in decreased survival, reproduction,
spat recruitment, and growth, and increased susceptibility
to diseases by P. marinus and MSX.
Rationale. Large rainfall events or large volume releases
from Lake Okeechobee (e.g., Caloosahatchee Estuary)
cause large volumes of freshwater over a short period of
time to enter the estuaries resulting in a sudden drop in
salinity. This abrupt reduction can lead to significant
mortality in the oyster population as well as decreased
growth, reproduction, and spat recruitment. Extreme
droughts can also negatively impact oysters by making
them more prone to disease and predation.
� Accumulation of muck (i.e., sediment with high organic
content) will render available substrate unsuitable for oyster
larval settlement and thus for recruitment and growth of
larval oysters. In addition, accumulation of muck may also
impact dissolved oxygen content making the substrate
unsuitable for larval settlement and growth.
Rationale. Oysters recruit successfully to immobile sandy
or shell-rich substrates, while recruitment is negatively
affected by the accumulation of mucky sediments.
Freshwater releases from the Lake and inland canals
Fig. 3 – Conceptual model of factors influencing oyster abundance and health in Southwest Florida estuaries. Factors in
dotted boxes are not currently being monitored but will be included in the future as information becomes available.
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6 S125
carry suspended sediments with silt, clay, and high
organic content soils. Freshwater inflow from canals can
also result in an increase in the transport of floating
plants, which then decompose and contribute to muck
accumulation.
� Increased sediment loads in the water column impair
respiration and feeding of oysters resulting in decreased
growth and condition index of oysters. In addition, sediment
accumulation negatively affects spat recruitment by render-
ing the substrate sub-optimal for larval settlement.
Rationale. Oyster populations are affected by increased
sediment loads resulting from alterations to the natural
hydrology and changes in land use. Adult oysters have
effective morphological and behavioral adaptations for
feeding when exposed to much higher levels of sus-
pended solids than are normally encountered. Oysters
from relatively turbid estuaries are capable of feeding in
waters with total suspended solid concentrations as high
as 0.4 g/l. However, this significantly reduces their
pumping rates at a sediment concentration as low as
0.1 g/l. Suspended solids may clog gills and interfere with
filtering and respiration of oysters.
� Increases in oyster-reef coverage will enhance secondary
habitat for other estuarine species resulting in increased
diversity and abundance.
Rationale. Oysters are natural components of southern
Florida estuaries and are documented as having been
historically abundant. Although currently less abundant,
they continue to be important. Reduction in oyster
coverage has been largely due to altered freshwater
inflow, shell mining, and changes in hydrology. These
perturbations have resulted in a loss of oyster reefs and
the communities they support.
1.4. Applicability of indicator to the Everglades
1.4.1. The indicator is relevant to the Everglades Ecosystemsand responds to variability at a scale that makes it applicable tothe entire estuarine portions of the ecosystemSeveral aspects of oysters, oyster reefs, and oyster-reef
communities make their use as an environmental indicator
relevant to estuarine portions of the Everglades Ecosystems.
Oysters are an estuarine species and their life cycle is typical of
many other species inhabiting estuaries. Water quality
conditions that influence oysters can therefore be expected
to influence other estuarine species in similar fashion
(Shumway, 1996). For these reasons oyster-reef survival,
distribution, and aerial extent are already key indicators
(performance measures) in RECOVER Conceptual Ecological
Models and in the CERP Interim Goals (Barnes, 2005; Sime,
2005).
Oysters and oyster reefs also provide a number of valuable
ecosystem services that in turn can be impacted by watershed
alteration and restoration. Oysters are primary consumers
relying on phytoplankton that forms the base of food chain in
the estuarine portions of the Everglades as well as other
estuaries (Newell, 1988; Volety and Savarese, 2001). As such,
oysters contribute to benthic–pelagic coupling through the
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6S126
deposition of phytoplankton and suspended detritus in the
form of mucus and uneaten food (Newell, 1988; Newell and
Langdon, 1996; Coen et al., 1999). Oyster reefs also provide
habitat, shelter, and food for over 300 species (Wells, 1961;
Coen et al., 1999). Many of the crustaceans and fishes that are
members of oyster-reef communities are important prey for
secondary and tertiary carnivores such as fishes and birds
(Tolley and Volety, 2005). Furthermore, biomass and commu-
nity structure of these oyster-reef communities are directly
linked to hydrology and oyster-reef survival and morphology
(Tolley et al., 2005, 2006).
1.4.2. The indicator is feasible to implement and isscientifically defensibleRelatively long-term data sets exist for oyster reefs at
numerous sites in Southwest Florida, spanning a course of 8
years in some cases (Volety, 2007), and there are existing
funded cooperative research and monitoring programs sup-
ported by RECOVER with Florida Gulf Coast University and the
Florida Fish and Wildlife Conservation Commission to con-
tinue this type of work. In addition, reliable models and
scientific studies exist to predict the impacts of water
management on these populations (Cake, 1983; Soniat and
Brody, 1988; Wilber and Bass, 1998; Livingston et al., 2000;
Barnes et al., 2007), and oysters have been included as part of
the CERP Habitat Suitability Index model (Volety et al., 2005).
Pattern metrics (e.g., abundance, density, survival, spat
recruitment, disease prevalence, and condition index) are
also statistically correlated to ecosystem drivers (Volety et al.,
2003; Volety, 2007).
1.4.3. The indicator is sensitive to system drivers (stressors)The peer-reviewed literature detailing the responses of
oysters to environmental stressors is somewhat extensive
(for reviews see Shumway, 1996; Kennedy, 1996). System
drivers (e.g., rainfall, water quantity, water quality, sediment
loads) have been statistically correlated to species abundance
and indicators of oyster health such as density, survival, spat
recruitment, disease prevalence, and condition index (Volety
et al., 2003; Wilber and Bass, 1998; Livingston et al., 2000; SSR,
2007). Oyster abundance, density, survival, and health indices
have been causally linked to hydrological factors such as
water salinity, the frequency of killing floods, sedimentation,
and contaminants in the water (Wilber and Bass, 1998;
Livingston et al., 2000; Volety et al., 2003; Bergquist et al.,
2006). As a result, high and low salinity estuaries have been
demonstrated to possess distinct oyster abundance, distribu-
tion, and health responses (Volety and Savarese, 2001; Volety
et al., 2003).
1.4.4. The indicator is integrativeOyster survival, abundance, and distribution are linked to
water quality, phytoplankton production, sedimentation, and,
in turn, crustacean, fish, and bird success are linked to oyster-
reef health and abundance (Cake, 1983; Reinhardt and Mann,
1990; Coen et al., 1999; Bergquist et al., 2006). Furthermore,
oyster-reef community responses are correlated with changes
in hydrology (e.g., salinity and freshwater inflow) and can
therefore be linked to water management (Tolley et al., 2005,
2006).
1.4.5. Goals and performance measures are established in theRECOVER MAP for the indicator and the following metrics arebeing monitored
� Number of live oysters per square meter.
� Number of acres of oyster reefs.
� Condition index of live oysters.
� Disease prevalence and intensity of P. marinus in oysters.
� Larval/spat recruitment and reproductive potential.
� Temperature and salinity of water near the reefs.
2. Communicating the oyster indicator
2.1. Methods and development of the indicator
The CERP MAP hypotheses related to the Eastern oyster and
how stressors impact them are detailed in Section 1. These
were derived through the development of the conceptual
model of the stressors influencing oysters (Fig. 3). As
previously mentioned, the oyster responses listed below
are being measured in all of the Northern Estuaries, but
the Caloosahatchee River will be used as an exemplar. The
results presented below are from six sampling locations
along the estuarine axis (salinity gradient) in the Caloosa-
hatchee Estuary collected over 5–7 years (Fig. 2). Sample
temporal trends are presented below; however, for the
sake of brevity detailed statistical analyses of the data
along with the temporal and spatial variation of oyster
responses are not presented. Details of the spatial and
temporal trends can be found in Volety et al. (2003),
Volety (2007), and SSR (2007). Since the objective of this
study is to use the available oyster performance data
from all five sampling locations in the CE to derive an
indicator score for the estuary, this study does not exa-
mine the causes of spatial and temporal variation of oyster
responses.
2.2. The metrics and performance measures
2.2.1. MetricsThe oyster indicator uses:
� density of living oysters (per square meter);
� condition index;
� reproductive activity (gonadal condition);
� larval recruitment;
� disease prevalence and intensity of P. marinus (and MSX in
east coast estuaries);
� growth and survival;
� coverage of oysters in the estuary (# acres).
2.2.2. Performance measures
� density of living oysters (per square meter);
� condition index;
� reproductive activity (gonadal condition);
� larval recruitment;
� disease prevalence and intensity of P. marinus (and MSX in
east coast estuaries);
� growth and survival.
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6 S127
All of these parameters are correlated with hydrological
conditions including depth, flow, salinity, temperature, dis-
solved oxygen, season, spatial extent, and water quality.
Salinity is a critical parameter in estuarine habitats. CERP
RECOVER targets for oyster performance measures are based
on patterns that are considered natural for the Northern
Estuaries along the east and west coasts of Florida.
3. Methods
3.1. The Stoplight Report Card system applied to oysters—determination of thresholds for success (green), caution(yellow) or failure (red)
The Stoplight Report Card system is a communication tool
that uses MAP performance measures to grade an estuary’s
response to anthropogenic or restoration inputs. Questions or
Table 1 – Decision rule questions for forming performance mecommunication tool
1. What is the current living density, in individuals per square meter, of
year (wet and dry season) sampling.
a. 0–200
b. >200–800
c. >800–4000
2. What is the current condition index of oysters in the Caloosahatchee
a. 0–1.5
b. >1.5–3.0
c. >3.0–6.0
3. What is the current gonadal condition of oysters in the Caloosahatche
a. 0–1
b. >1–2
c. >2–4
4. What is the current spat recruitment of oysters (spat/shell) in the Cal
monthly sampling.
a. 0–5
b. >5–20
c. >20–200
5. What is the current growth of juvenile oysters in mm/month? Use ye
a. 0–1
b. >1.0–2.5
c. >2.5–5
6. What is the prevalence of Perkinsus marinus (% of infected oysters) in
monthly sampling.
a. 0–20
b. >20–50
c. >50–100
7. What is the intensity of Perkinsus marinus (scale 0–5) in oysters from
sampling.
a. 0–1
b. >1–3
c. >3–5
Trend question
a. � slope
b. No slope
c. + slope
A score of 1.0 for a performance measure is the restoration target. All per
the data availability at various estuaries (5–8 years) and is presented sep
decision rules are developed for each performance measure
and translated as suitability curves. Two questions are
addressed using suitability curves: (1) Have we reached the
restoration target? And (2) are we making progress toward
targets? Finally, results are translated into a stoplight display
(see below for example).
The system-wide indicator communication tool is based on
RECOVER MAP ecological attributes and performance mea-
sures. This communication tool has been designed to
distinguish between the effects of restoration projects and
natural phenomena, assuming that the available data cover
periods of high, normal, and low rainfall (and inflow) years.
Targets for performance measures are established from
historical data or reference sites. By using spatially referenced
suitability indices the indicator communication tool can be
linked directly to both the RECOVER evaluation and assess-
ment processes and the Task Force indicator assessments.
The communication tool instantly conveys the status of the
asure/suitability relationships for the oyster indicator
oysters in the Caloosahatchee Estuary. Use yearly average of twice a
Score: 0 Red
Score: 0.5 Yellow
Score: 1.0 Green
Estuary? Use the yearly average of monthly sampling.
Score: 0 Red
Score: 0.5 Yellow
Score: 1.0 Green
e Estuary? Use the yearly average of monthly sampling.
Score: 0 Red
Score: 0.5 Yellow
Score: 1 Green
oosahatchee Estuary? Use mean spat/shell/month for the estuary of
Score: 0 Red
Score: 0.5 Yellow
Score: 1.0 Green
arly average of monthly sampling.
Score: 0 Red
Score: 0.5 Yellow
Score: 1.0 Green
oysters from the Caloosahatchee Estuary? Use the yearly average of
Score: 1 Green
Score: 0.5 Yellow
Score: 0 Red
the Caloosahatchee Estuary? Use the yearly average of monthly
Score: 1 Green
Score: 0.5 Yellow
Score: 0 Red
Score: 0 Red
Score: 0.5 Yellow
Score: 1.0 Green
formance measures are averages of 2–5 years. The trend is based on
arately.
Fig. 4 – Example of linear suitability curve for an oyster
indicator performance measure (living density). The x-axis
varies for each performance measure as described in
Table 1.
Fig. 5 – Example of trend curves for a oyster performance
measure (living density). The green line is a positive trend
and gets a score of 1.0; the yellow line indicates no change
and is scored 0.0; and the red line is a negative trend (away
from the target) and is scored 0.0.
Table 2 – Translation table for converting the suitabilityor trend index for a performance measure or indicatorinto an index score and stoplight color
Index range Index score Stoplight color
0.0–0.3 0 Red
>0.3–0.6 0.5 Yellow
>0.6–1.0 1.0 Green
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indicator, and the suitability and trend curves provide infor-
mation on progress towards reaching a target. This indicator
communication tool has the advantage of being able to be
applied regionally, by species, and collectively system-
wide. Importantly, both targets and suitability curves can be
adapted as science improves our understanding of Greater
Everglades Ecosystems.
Oyster response data for various metrics are available for
5–7 years for the Caloosahatchee Estuary and were thus
chosen as an illustrative example. Tables 1 and 2 present the
decision rules used to create the suitability scores. Data in
excess of 5 years are not available for all of the responses
being measured; therefore, in addition to available data
(Table 4), a hypothetical data set using the ranges of oyster
responses in the Caloosahatchee Estuary was also used to
generate an index score (Fig. 4) and a trend score (Fig. 5)
(Table 3). For most of the oyster performance measures
empirical data were used from study sites (Volety, 2007;
Systems Status Report, 2007). Both targets and curves can be
modified as more is learned about this indicator. Trends for
each performance measure are determined from a five-year
plot of the performance measure (Fig. 5). All metrics were
measured at each station monthly while the living density
was measured twice a year (wet and dry seasons). The
component score (e.g., living density) is the average of the
suitability index score and the trend score (Table 1). Tables 3
and 4 provide a hypothetical example of how component
scores can be combined into a system-wide indicator score.
3.2. Oyster metrics
3.2.1. Water quality determination and relationship betweenfreshwater inflows and salinityWater quality measurements were taken in association with
sample collection (oysters) using a YSI data sonde. Tempera-
Table 3 – Hypothetical example of translating performance m
Component Parametervalue
Parametervalue
stoplight
Indexscore
Oysters
Living density (per m2) 50 0
Condition index 2.3 0.5
Spat recruitment per shell 2 0
Juvenile growth (mm) 2 0.5
Perkinsus marinus prevalence 15 1
Perkinsus marinus intensity 1.5 0.5
Geometric mean of oyster component scores
(0.5 � 0.25 � 0.25 � 0.5 � 1 � 0.75)1/6 = 0.477
Final Eastern oyster index score = 0.5
ture, salinity, and dissolved oxygen were measured at the
surface (given the shallowness of the environment). Fresh-
water inflows (cubic feet per second; cfs) into the Caloosa-
hatchee Estuary from S-79 lock and dam were obtained from
easures into a stoplight display
Trend Trendstoplight
Trendscore
Averagecomponent
score
Componentstoplight
+ 1 (0 + 1)/2 = 0.5
� 0 (0.5 + 0)/2 = 0.25
� 0.5 (0 + 0.5)/2 = 0.25
� 0.5 (0.5 + 0.5)/2 = 0.5
+ 1 (1 + 1)/2 = 1
+ 1 (0.5 + 1)/2 = 0.75
Table 4 – Component score for oysters in the Caloosahatchee Estuary for translating performance measures into astoplight display
Component Parametervalue
Parametervalue
stoplight
Indexscore
Trend Trendstoplight
Trendscore
Averagecomponent
score
Componentstoplight
Oysters
Living density (per m2) 1029 1 � 0.5 (1 + 0.5)/2 = 0.75
Condition index 2.96 0.5 � 0.5 (0.5 + 0.5)/2 = 0.5
Gonadal Index 2.61 1 � 0.5 (1 + 0.5)/2 = 0.75
Spat recruitment per shell 6.43 0.5 � 0.5 (0 + 0.5)/2 = 0.5
Juvenile growth (mm/month) 2 0.5 � 0.5 (0.5 + 0.5)/2 = 0.5
Perkinsus marinus prevalence 49.5 0.5 � 0 (0.5 + 0)/2 = 0.25
Perkinsus marinus intensity 0.83 1 � 0 (1 + 0)/2 = 0.5
Geometric mean of oyster component scores
(0.75 � 0.5 � 0.75 � 0.5 � 0.5 � 0.25 � 0.5)1/7 = 0.508
Final Eastern oyster index score = 0.5
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the South Florida Water Management District (courtesy of Dr.
P. Doering and K. Haunert). The relationship between fresh-
water inflow and salinity at various sampling locations was
determined using power regressions (SPSS). Salinity at various
sampling locations obtained during the sampling period was
regressed against the 30-day moving average flows for the
sampling month.
3.2.2. Estimating oyster density
Density of living oysters, an indirect measure of reef
productivity, also varies considerably along an estuarine
salinity gradient. Patterns attributable to human alterations
in freshwater flow were detected previously in the Black-
water and Faka Union estuaries of the Ten Thousand
Islands (Volety and Savarese, 2001). Oyster living density at
CE sampling stations was measured during the late fall and
early spring every year. This period is ideal for density
measurement because oysters have reproduced for the year
and spat have settled from the water column. Four 0.25-m2
quadrats were randomly located at the mean-low-tide
height at each reef. The number of living oysters within
each quadrat were counted and compared among reefs at
various locations.
3.2.3. Determining oyster condition indexThe physiological condition of an oyster can be measured
by its condition index—the ratio of meat weight to shell weight
(Lucas and Beninger, 1985). Although oysters tolerate salinities
between 0 and 42 ppt, growth is maximized at salinities of 14–
28 ppt; slower growth, poor spat production, and excessive
valve closure occur at salinities below 14 ppt (Shumway, 1996).
Because the metabolic energy remaining after daily main-
tenance is converted into biomass, an oyster stressed either by
poor water quality or by disease has less energy for growth or
reproduction. Consequently, a comparison of oyster condition
index among oyster reefs located along the salinity gradient
should be indicative of oyster health and the influence of
salinity and disease. Oysters from an altered estuary having
extreme salinities have significantly lower condition index
compared to oysters from an unaltered estuary (Volety and
Savarese, 2001). Oysters were collected for condition index
determination monthly at the same time disease prevalence
was surveyed.
3.2.4. Gonadal IndexHistological analysis was used to examine gonadal state and
reproductive potential of oysters from different sites (see
above) during the study period. Gametogenic stage was
identified under a microscope according to Fisher et al. (1996)
and the International Mussel Watch Program (1980). Samples
of 10–15 oysters were collected monthly from each sampling
location. For histological sectioning, a 3–5 mm thick band
of tissue was cut transversely with a razor blade in such a
manner as to contain portions of mantle, gill, digestive
tubule, and gonad. Dissected tissue was fixed for 48–72 h in
Davidson’s fixative and stored in 70% ethanol before paraffin
embedding. After embedding, sections were made with a
microtome, and slides were stained with hematoxylin and
eosin. Gonadal portions of the sections were observed by light
microscopy to determine sex and gonadal condition (Fisher
et al., 1996).
A description of gametogenic characteristics (reproductive
staging) observed in histological sections of oyster gonads and
the values assigned for the determination of gonadal condi-
tion are presented in Appendix 1 (International Mussel Watch
Program 1980; Fisher et al., 1996). Values of 6–10 were
converted to 5–1 to reflect true reproductive activity (similar
% of mature gametes in the follicles) for statistical purposes.
For example, in a random sample, if five oysters are at stage 1
and 5 oysters at stage 10, stages that have no mature gametes,
when averaged the value is 5.5, which erroneously suggests
that oysters are actively spawning. Changing the values from 6
to 10 would yield values that accurately reflect the reproduc-
tive stage of the oysters (Volety and Savarese, 2001; Volety
et al., 2003).
3.2.5. Spat recruitmentOyster spat recruitment experiments were conducted using
old adult oyster shells strung together by a weighted
galvanized wire and deployed at sampling locations. A shell
string consisting of 12 oyster shells, each 5.0–7.5 cm long with
a hole drilled in the center and oriented inner surface down,
was suspended off the bottom at various sites (Haven and
Fritz, 1985). Oyster spat settlement was monitored monthly by
counting the number of spat settled on the underside of strung
shells. Spat settlement is expressed as the number of spat
settled per oyster shell per month.
Fig. 7 – Mean condition index of oysters from all the
sampling locations in the Caloosahatchee Estuary. 10–15
oysters were collected monthly from each of the sampling
locations between August 1999 and January 2008.
Fig. 6 – Relationship between freshwater inflows into the
Caloosahatchee Estuary and salinities at various points in
the estuary. Monthly means of the 30-day moving average
salinity were regressed against salinity from the sampling
locations. Results suggest that increasing freshwater
inflow decreases the salinities at various locations in the
estuary.
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3.2.6. Juvenile oyster growth and survivalOne to two hundred juvenile oysters (10–20 mm) were
deployed at all sampling locations in 0.5 mm closed wire-
mesh bags in the fall months (a period that coincides with
natural spawning period). Fifty randomly selected oysters
were measured to the nearest 0.1 mm every month from each
location. Juvenile oysters were placed at the sampling
locations in wire-mesh bags to exclude predation and indicate
growth and/or mortality due to water quality.
3.2.7. Estimating oyster disease prevalence and distributionP. marinus disease susceptibility in oysters along the salinity
gradient within the Caloosahatchee Estuary was determined
at six locations. A total of 10–15 oysters per location were
collected monthly throughout the year. Oysters were assayed
for the presence of P. marinus using Ray’s fluid thioglycollate
medium technique (Ray, 1954; Volety et al., 2000, 2003).
Samples of gill and digestive diverticulum were incubated in
the medium for 4–5 days. P. marinus meronts enlarge in the
medium and stain blue-black with Lugol’s iodine allowing
for visual identification under a microscope. Prevalence of
infection was calculated as % infected oysters. The intensity of
infection was recorded using a modified Mackin scale (Mackin,
1962) in which 0 = no infection, 1 = light, 2 = light-moderate,
3 = moderate, 4 = moderate-heavy, 5 = heavy.
4. Results
4.1. Water quality determination and relationshipbetween freshwater inflows and salinity
As expected, temperatures at the sampling locations in the CE
were higher during the warmer summer—early fall months
(April–October) and were lower during the cooler drier months
(November–March). In contrast, salinities at sampling loca-
tions were lower during the summer—early fall months (June–
October) and higher during the cooler months (November–
May; results not shown). There was a significant relationship
between flows and salinity at the five sampled locations
(P < 0.001; R2 = 53–75% depending on the sampling location;
Fig. 6). The influence of freshwater inflow on the system is
more pronounced at the upstream locations compared to the
downstream locations.
4.2. Oyster density
Inter-annual variation of oyster density ranged between 102
and 2345 oysters m�2 at various sampling locations. Because
density data were only available for two years, a trend analysis
was not computed. Mean density for all the sampling locations
in the CE in 2006 and 2007 ranged from a low of 710 � 663 (2006
wet season) to a high of 1296 � 997 oysters m�2 (dry season
2006).
4.3. Oyster condition index
Condition index of oysters varied significantly among sam-
pling locations and sampling months (P < 0.001). Condition
index in oysters was higher from December to May and lowest
in October. Condition index decreased through March–
October (Fig. 7), a period that coincided with oyster spawning.
4.4. Gonadal stage
Gonadal Index, a measure of the reproductive stage of
spawning oysters, was very cyclical and varied significantly
among sampling locations and sampling months (P < 0.001).
Gonadal Index was higher during April–October, suggesting
active spawning of oysters, and lower during November–
March (Fig. 8).
4.5. Spat recruitment
Spat recruitment of oysters varied significantly among samp-
ling locations and sampling months (P < 0.001). Recruitment
Fig. 11 – Mean intensity of Perkinsus marinus in oysters
from all the sampling locations in the Caloosahatchee
Estuary. 10–15 oysters were collected monthly from each
of the sampling locations between August 1999 and
Fig. 8 – Mean gonadal stage of oysters from all the sampling
locations in the Caloosahatchee Estuary. 10–15 oysters
were collected monthly from each of the sampling
locations between August 1999 and September 2007.
Fig. 10 – Mean prevalence of Perkinsus marinus (% of
infected oysters) from all the sampling locations in the
Caloosahatchee Estuary. 10–15 oysters were collected
monthly from each of the sampling locations between
August 1999 and January 2008.
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6 S131
of spat was higher from April to October, with peak recrui-
tment occurring in August. Little or no spat recruitment was
observed between November and March (Fig. 9).
4.6. Juvenile oyster growth
Juvenile oyster growth and mortality varied widely among
sampling locations and sampling months. Significant juvenile
mortality was observed when oysters were deployed during
the summer months when salinities were typically low
(results not shown). When oysters were deployed in late fall
months (October to December) when salinities were higher,
faster growth was observed at the upstream locations, which
tended to have more estuarine salinities, compared to down-
stream locations where salinities were marine to hypersaline.
Mortality rates were typically 60–100% depending on salinity
(results not shown).
Fig. 9 – Mean spat recruitment (spat/shell) of oysters from
all the sampling locations in the Caloosahatchee Estuary.
Data were collected monthly from each of the sampling
locations between August 1999 and January 2008.
January 2008.
4.7. Oyster disease prevalence and intensity
Disease prevalence (Fig. 10) and intensity (Fig. 11) of P. marinus
varied significantly (P < 0.001) among sampling locations and
sampling months. Disease prevalence and intensity increased
with increasing salinity and distance downstream (results not
shown). On average, disease prevalence and intensity were
higher in January (when salinities tend to be higher) and
August (when temperatures tend to be the highest).
5. Discussion
The RECOVER Conceptual Ecological Models identify three
major stressors that affect the success of Eastern oysters and
associated invertebrate and vertebrate species: altered hydrol-
ogy, altered habitat (affecting habitat loss, hydrology, water
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quality), and sedimentation (affecting habitat loss) (CERP
MAP 2004). Land development around the watersheds of the
Northern (and Southern) Estuaries represents a large loss of
habitat given the watershed runoff and resulting low salini-
ties, as well as poor water quality (e.g., contaminants, bacteria,
sedimentation). This loss has had a major negative impact on
oyster reefs and has thus indirectly and directly impacted
macroinvertebrate and fish species.
Water management activities within these watersheds have
resulted in significant alterations in the timing (excess wet
season and insufficient dry season water flows), distribution
(water now flows through canals instead of overland), volume,
and quality of water delivered to these estuaries. Channeliza-
tion and water control structures have reduced the ability of
these systems to filter nutrients and have led to further
degradation of water quality. These impacts reduce water
storage in the watershed, dry season flows, water-quality
treatment, and fish and wildlife habitat. Pre-drainage estuarine
systems received freshwater inflow primarily from direct
rainfall and slow basin runoff that resulted in low nutrient
inputs. These natural patterns of freshwater inflow sustained
an ecologically appropriate range of salinity conditions with
fewer salinity extremes. Water management and dredging
practices have had major impacts on the presence of oysters
within these estuaries. CERP projects that will restore more
natural freshwater inflows into the estuaries will provide
beneficial salinity conditions, a reduction in nutrient concen-
trations and loads,and improved water clarity thatwill promote
the reestablishment of healthy oyster bars and associated
communities. These stressors and attributes are described in
the conceptual ecological models in the RECOVER MAP.
In the present study, the Caloosahatchee Estuary was
chosen as a model estuary to examine the impact of
watershed alteration on oysters and to develop a Stoplight
Report Card for oyster physiological and ecological response.
The CE encounters high freshwater inflows due to local
rainfall events and large regulatory freshwater releases from
Lake Okeechobee, depressing salinities for extended periods.
However, large extended regulatory releases are not a natural
event and can result in harmful reductions in salinities for
extended periods. A significant relationship between fresh-
water inflows and salinities at all the sampling sites was noted
in areas where oyster reefs naturally exist. Results suggest
that flows between 500 and 3500 cfs will result in salinities
between 10 and 32 ppt (Fig. 6), a range that is favorable to
oysters (Shumway, 1996; Volety et al., 2003). Adult oyster
density, substrate availability and suitability for larval oyster
spat recruitment, disease intensity and prevalence of P.
marinus, condition of oysters, reproduction, and susceptibility
to predation are all influenced by the timing, duration, and
frequency of freshwater flows into the estuaries. Average
oyster condition index ranged between 2.4 and 3.4 in the CE
(Fig. 7), with changes coinciding with the reproductive phase
of oysters. As oysters reproduce, gametes are shed resulting in
a decrease in body mass and thus a reduced condition index.
This trend is reinforced by seasonal patterns in oyster Gonadal
Index and spat recruitment. The Gonadal Index of oysters was
higher during peak spawning months (April–October; Fig. 8).
Larval recruitment was observed at various sampling loca-
tions between April and October (Fig. 9). Spat recruitment per
shell ranged between 2.5 and 25, suggesting that the CE is not
limited by larval availability. Juvenile oysters grow faster than
adult oysters, thus enabling the determination of growth rates
at various locations subjected to various salinities.
Given the variation of freshwater inflow into the CE (0 –
15,000 cfs), growth and survival of oysters was significantly
impacted at the extreme end of the salinity range, and varied
with time of deployment. Given the variability in the time of
deployment, growth rates and survival of juvenile oysters due
to ambient salinity, data could not be statistically analyzed for
this study. Mean P. marinus prevalence from all the sampling
locations and sampling months ranged from 31 to 66% (Fig. 10)
between sampling months (when data are combined from all
the sampling stations) and between 35 and 56% among
sampling locations (when data are combined from all the
sampling locations; results not shown) to represent the
current data and trends. Similarly, P. marinus intensity ranged
between 0.64 and 1.16 during various sampling months (scale
0–5; Fig. 11) and between 0.41 and 1.1 at various sampling
locations (results not shown). These results were used to
develop an easy to understand Stoplight Report Card system to
characterize the current state of oysters in the Caloosahatchee
Estuary, and not to examine the relationship between various
water management practices and interrelationships between
oyster responses and other factors that influence them.
Based on the available data of oyster responses in the
Caloosahatchee Estuary, the system appears to be at stage
‘‘caution’’ (yellow). This level may change as modifications to
the system occur (e.g., change in the quality, quantity, timing
and distribution of freshwater inflows) as CERP projects are
implemented. In the current study, all the metrics monitored
were weighted equally in determining the Component Score;
however, in other systems, various responses may be dropped
or weighted more or less, as appropriate.
Suitability indices can bridge the gap between the Task
Force’s System-wide Indicators (Barnes et al., 2007) and the
RECOVER MAP process. When combined with spatially
referenced maps of an indicator (ecological attribute in the
MAP Conceptual Ecological Models), indicator performance
measure suitability curves can provide a basis for restoration
project evaluation or assessment. Combined with a scoring
system and stoplight display (as part of a more detailed
scientific report) the suitability curves form the basis for the
communication tool (Table 2). Translating index scores into a
stoplight display can be done for each performance measure
(component) and then combined into a species score (e.g.,
Eastern oyster) by MAP module, and then each species
individually system-wide to provide a system-wide oyster
indicator score.
The Northern Estuaries CERP oyster indicator targets are
based on optimization model outputs, natural variation that
did occur during the period 1965–2000, and desirable salinity
conditions for existing and potential aquatic resources (CERP-
MAP, 2004). Targets for the CE are based on freshwater
discharges from the C-43 canal at the S79 structure where
the mean monthly inflow should be maintained between 450
and 2800 cfs. Targets were developed to better manage
minimum and maximum flow events to the estuary to
improve estuarine water quality, and to protect and enhance
estuarine habitat and biota.
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5.1. Low flow
The low flow target is no months from October to July when
the mean monthly inflow from the Caloosahatchee water-
shed, as measured at S79, falls below a limit of 450 cfs (C-43
basin runoff and Lake Okeechobee regulatory releases).
5.2. High flow
The high flow target is no months with mean monthly flows
greater than 2800 cfs, as measured at the S79, from Lake
Okeechobee regulatory releases in combination with flows
from the Caloosahatchee River (C-43) basin.
5.3. Frequency and rates of flows
The frequency distribution of monthly average freshwater
inflows through S-79 for the entire period of record has been
found to be important for protecting and restoring estuarine
resources. Approximately 75% of the flows from S79 should be
in the 450–800 cfs range and most of the remaining inflow
should be in 800–2800 cfs range.
5.4. Lake Okeechobee regulatory releases
The alternative with the least daily discharge volume, the
fewest number of total days of discharge, and the fewest
number of consecutive days of discharge is preferred. Special
considerations are provided for pulsed releases that benefit
the estuary.
5.5. Optimal flows in the Caloosahatchee Estuary
Volety et al. (2003) recommended freshwater inflows for the
protection and enhancement of oyster recruitment and
survival around Shell Point and San Carlos Bay that are
consistent with the flows outlined above and for SAV. Flows
between 500 and 2000 cfs would result in salinities of 12–30 ppt
at all stations, conditions that are favorable to sustain and
enhance oyster populations in the Caloosahatchee Estuary.
Under current water management practices, oysters in the
Caloosahatchee are not stressed by low flows of<300 cfs from
S79; however, complete cessation of discharges during the
winter will increase salinities in areas normally associated
with lower salinity and result in the immigration of marine
predators and pests. Volety et al. (2003) further speculate that
oyster spat in downstream areas also will be exposed to higher
salinity and heavy predation pressure resulting in very little
survival.
Nonetheless, the greatest threat to oysters under current
water management practices is due to high flows exceeding
3000 cfs for extended periods (2–4 weeks). This is especially
true for summer months during peak oyster spawning,
juvenile recruitment, and growth. Volety et al. (2003) recom-
mended that although freshwater releases may still be
necessary prior to CERP, repeated pulses of <1 week duration
during winter months should be made instead of sustained
releases of freshwater during summer or winter months.
Interpretation of these results also indicates that such pulses
would be least damaging during December through February,
before increased spawning and recruitment begins at
upstream locations. Salinities preferred by oysters will be
maintained if the target flow frequency distribution is
achieved, especially if 75% of the flows are between 450 and
800 cfs. In addition to the freshwater inflow resulting from
regulatory lake releases, natural events such as tropical
storms and hurricanes contribute to significant amount of
rainfall and watershed runoff resulting in depressed salinities.
However, the residence time of freshwater resulting from
these events is relatively short (1–3 days), compared to the
regulatory releases which could last for several weeks, and
thus have a minimal impact on oyster responses.
The CERP goal for the Northern Estuaries is to enhance
habitat conditions while providing for economic and recrea-
tional opportunities. CERP projects are expected to moderate
the stressors (i.e., freshwater discharges, diminished water
quality, and habitat loss) and enhance the natural attributes
(i.e., oysters) of the Northern Estuaries. This will be accom-
plished through habitat enhancement, as well as through water
storage and treatment projects. As various CERP projects are
implemented, changes in the hydrology, and thus the biology of
oysters will take place. Provided that sufficient data covering
normal variability in rainfall and temperature events (normal,
dry and wet years; hot and cool years) exist, a Stoplight Report
Card system that integrates various responses that are
currently being measured as part of a monitoring plan can
provide a powerful way to distinguish between restoration
changes and natural patterns. For example, the existing
data (that can be enhanced by continuous monitoring)
will provide ranges of oyster responses. Comparing oyster
responses after restoration-related alterations have taken place
with normal ranges (prior to restoration), one can distinguish
whether restoration activities are enhancing or diminishing
oyster responses.
6. Longer term science needs
The oyster monitoring protocol metrics currently include
changes in oyster distribution and abundance at a variety of
estuarine sites on both the east and west coasts of Florida,
including the St. Lucie Estuary, Caloosahatchee Estuary,
Loxahatchee River, and Lake Worth Lagoon. This long-term
monitoring program for the Eastern oyster focuses on four
aspects of oyster ecology: spatial and size distribution patterns
of adults, distribution and frequency patterns of diseases,
reproduction and recruitment, and juvenile growth and
survival. The current monitoring protocol for oysters in the
Northern Estuaries provides a good starting point to assess the
current state of oysters, evaluating the baselines responses
(pre-CERP alterations). Data will be analyzed to determine if
the health and spatial extent of oysters is improving with time
as CERP projects are implemented and if the predictions for
the oyster Interim Goal are being met.
The responses measured are based on the rationale
previously provided; however, several improvements can
be made to the existing monitoring protocol. For example,
water quality (i.e., temperature, salinity, and DO) is being
measured at all the sampling sites during each sampling
event (once a month). However, a more frequent sampling is
e c o l o g i c a l i n d i c a t o r s 9 s ( 2 0 0 9 ) s 1 2 0 – s 1 3 6S134
required to capture episodic events. In addition, predation
pressure may be a significant factor in the survival of oysters,
and is currently not being studied. Given that predation
pressure is anticipated to be high in some locations, such
information is necessary and will enhance the Habitat
Suitability Index (HSI) model by strengthening the predict-
ability of potential suitable habitat.
A Habitat Suitability Index model (HSI) is currently under
development for oysters in the Northern Estuaries. This GIS-
linked HSI will enable resource managers to make compar-
isons between different scenarios enhancing the decision-
making process. Basic information about salinity changes and
their impacts on oysters and associated communities is
relatively well understood. However, these data are mostly
from areas outside the Northern Estuaries. Oysters are
adapted to local conditions, and therefore their responses to
ambient environmental conditions in the Northern Estuaries
may be different. Continued work is needed to standardize the
measurements between estuaries and continue to capitalize
on developing time-series information on oysters in various
estuaries.
The sample size for each of the performance metrics is partly
dictated by sample collection and processing time as well as
expense. For example, analyses of reproduction are currently
performed using histological techniques. Such techniques are
time-consuming, expensive and require specific expertise
limiting the number of samples that can be analyzed. Newer
techniques such as enzyme-linked immunosorbant assay that
use antibodies against egg protein of Eastern oysters are now
being developed. These techniques will greatly enhance the
sample processing and increase the sample size and thus the
power of the analyses.
Although some factors that influence oyster responses
are not being measured in the current study, their influence
in the success of oyster reefs in these estuaries will be
examined in the future, based on need. In addition, use of
newer tools such as Habitat Suitability Index models (Barnes
et al., 2007) will shed light on some of the factors influencing
oyster growth and survival, which can then be included in
the monitoring plan. Factors that are not currently exam-
ined but may have potential influences on oysters and those
that may be examined at a later time are indicated by
dashed boxes in the conceptual model. Predictions of
oyster-reef development following implementation of
CERP can be made by using a HSI model (Barnes et al.,
2007). Although the existing sampling design and sampling
frequency can adequately assess the direction and magni-
tude of change in the performance measures of oysters, the
sampling protocol may be adjusted to better capture the
spatial variation of responses. The Stoplight Report Card
system, in concert with HSIs such as those developed for
oysters by Cake (1983), Soniat and Brody (1988), and Barnes
et al. (2007) will enable resource managers to enhance
decision making by providing them with a powerful tool
that is based on real scientific data rather than relying solely
on informal judgments or professional opinion. These
models can then provide input and direction for monitoring
efforts. These approaches are also easily exportable for use
in other estuaries in Florida and other Gulf states with
minor modifications.
Acknowledgments
This study was made possible by funding from the South
Florida Water Management District (Grant nos. C-12412-A1
and CP 040626) and the US EPA. We would like to acknowledge
the field and lab and logistical assistance of our lab staff Ms.
Sharon Thurston, Lesli Haynes, Erin Dykes, Amanda Booth,
and Christal Niemeyer. Numerous graduate and undergrad-
uate students have contributed to the lab and field work. Many
of these interns were supported by Congressional Grant
P116Z010066 awarded through the U.S. Department of Educa-
tion and Congressional Grant X7-96403504-0 awarded through
the U.S. Environmental Protection Agency. Without the
assistance of the lab staff and students, this project would
not have been made possible. Comments from Drs. Philippe
Soudant, Jerome La Peyre and Megan La Peyre on earlier drafts
have significantly improved the manuscript. We thank Greg
May, the Executive Director of the South Florida Ecosystem
Restoration Task Force and Rock Salt, Co-chair of the Science
Coordination Group, for their support in making the publica-
tion of this special issue of Ecological Indicators possible.
Appendix 1
Gonadal stage Observations
0 Neuter or resting stage with no visible signs
of gametes
1 Gametogenesis has begun with no mature
gametes
2 First appearance of mature gametes to
approximately one-third mature gametes
in follicles
3 Follicles have approximately equal proportions
of mature and developing gametes
4 Gametogenesis progressing, but follicles
dominated by mature gametes
5 Follicles distended and filled with ripe gametes,
limited gametogenesis, ova compacted into
polygonal
configurations, and sperm have visible tails
6 = 5 Active emission (spawning) occurring; general
reduction in sperm density or morphological
rounding of ova
7 = 4 Follicles one-half depleted of mature gametes
8 = 3 Gonadal area is reduced, follicles two-thirds
depleted of matures gametes
9 = 2 Only residual gametes remain, some cytolysis
evident
10 = 1 Gonads completely devoid of gametes, and
cytolysis is ongoing
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